Home LiteratureArticle Details
PMID: 21551351 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Integration of the genetic map and genome assembly of fugu facilitates insights into distinct features of genome evolution in teleosts and mammals.

Genome biology and evolution ·Vol. 3 ·2011-00-00 ·Pages 424-42

Kai W, Kikuchi K, Tohari S, Chew AK, Tay A, Fujiwara A, Hosoya S, Suetake H, Naruse K, Brenner S, Suzuki Y, Venkatesh B

Abstract

The compact genome of fugu (Takifugu rubripes) has been used widely as a reference genome for understanding the evolution of vertebrate genomes. However, the fragmented nature of the fugu genome assembly has restricted its use for comparisons of genome architecture in vertebrates. To extend the contiguity of the assembly to the chromosomal level, we have generated a comprehensive genetic map of fugu and anchored the scaffolds of the assembly to the 22 chromosomes of fugu. The map consists of 1,220 microsatellite markers that provide anchor points to 697 scaffolds covering 86% of the genome assembly (http://www.fugu-sg.org/). The integrated genome map revealed a higher recombination rate in fugu compared with other vertebrates and a wide variation in the recombination rate between sexes and across chromosomes of fugu. We used the extended assembly to explore recent rearrangement events in the lineages of fugu, Tetraodon, and medaka and compared them with rearrangements in three mammalian (human, mouse, and opossum) lineages. Between the two pufferfishes, fugu has experienced fewer chromosomal rearrangements than Tetraodon. The gene order is more highly conserved in the three teleosts than in mammals largely due to a lower rate of interchromosomal rearrangements in the teleosts. These results provide new insights into the distinct patterns of genome evolution between teleosts and mammals. The consolidated genome map and the genetic map of fugu are valuable resources for comparative genomics of vertebrates and for elucidating the genetic basis of the phenotypic diversity of ~25 species of Takifugu that evolved within the last 5 My.

MeSH Terms
Animals Chromosome Mapping Chromosomes Conserved Sequence/genetics Evolution, Molecular Gene Order Gene Rearrangement Genome Humans In Situ Hybridization, Fluorescence Mammals/genetics Mice Microsatellite Repeats Opossums/genetics Oryzias/genetics Phylogeny Sequence Analysis, DNA Takifugu/genetics Tetraodontiformes/genetics
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Kai Wataru
Fisheries Laboratory, Graduate School of Agricultural and Life Sciences, University of Tokyo, Hamamatsu, Shizuoka, Japan.
Kikuchi Kiyoshi
Tohari Sumanty
Chew Ah Keng
Tay Alice
Fujiwara Atushi
Hosoya Sho
Suetake Hiroaki
Naruse Kiyoshi
Brenner Sydney
Suzuki Yuzuru
Venkatesh Byrappa
References (66)
66 references, click to expand
  1. Improved fish lymphocyte culture for chromosome preparation.
    Genetica. 2001;111(1-3):77-89 PMID: 11841191
  2. The medaka draft genome and insights into vertebrate genome evolution.
    Nature. 2007 Jun 7;447(7145):714-9 PMID: 17554307
  3. Explosive speciation of Takifugu: another use of fugu as a model system for evolutionary biology.
    Mol Biol Evol. 2009 Mar;26(3):623-9 PMID: 19074759
  4. Global patterns of human DNA sequence variation in a 10-kb region on chromosome 1.
    Mol Biol Evol. 2001 Feb;18(2):214-22 PMID: 11158380
  5. Takifugu obscurus is a euryhaline fugu species very close to Takifugu rubripes and suitable for studying osmoregulation.
    BMC Physiol. 2005 Dec 20;5:18 PMID: 16364184
  6. Steps in the evolution of heteromorphic sex chromosomes.
    Heredity (Edinb). 2005 Aug;95(2):118-28 PMID: 15931241
  7. Evolution of genes and genomes on the Drosophila phylogeny.
    Nature. 2007 Nov 8;450(7167):203-18 PMID: 17994087
  8. Duplication events and the evolution of segmental identity.
    Evol Dev. 2005 Nov-Dec;7(6):556-67 PMID: 16336409
  9. The evolution of sex dimorphism in recombination.
    Genetics. 2003 Feb;163(2):811-22 PMID: 12618416
  10. Rates of nucleotide substitution in primates and rodents and the generation-time effect hypothesis.
    Mol Phylogenet Evol. 1996 Feb;5(1):182-7 PMID: 8673286
  11. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes.
    Science. 2002 Aug 23;297(5585):1301-10 PMID: 12142439
  12. Comparative genomics using Fugu reveals insights into regulatory subfunctionalization.
    Genome Biol. 2007;8(4):R53 PMID: 17428329
  13. The zebrafish gene map defines ancestral vertebrate chromosomes.
    Genome Res. 2005 Sep;15(9):1307-14 PMID: 16109975
  14. The Origin of Interspecific Genomic Incompatibility via Gene Duplication.
    Am Nat. 2000 Dec;156(6):590-605 PMID: 29592543
  15. Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene.
    Genetics. 2007 Dec;177(4):2075-81 PMID: 17947439
  16. Evolution of Otx paralogue usages in early patterning of the vertebrate head.
    Dev Biol. 2009 Jan 1;325(1):282-95 PMID: 18848537
  17. A high-resolution recombination map of the human genome.
    Nat Genet. 2002 Jul;31(3):241-7 PMID: 12053178
  18. Comparison of C. elegans and C. briggsae genome sequences reveals extensive conservation of chromosome organization and synteny.
    PLoS Biol. 2007 Jul;5(7):e167 PMID: 17608563
  19. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates.
    Genome Res. 2007 Sep;17(9):1254-65 PMID: 17652425
  20. The evolutionary fate and consequences of duplicate genes.
    Science. 2000 Nov 10;290(5494):1151-5 PMID: 11073452
  21. A new time-scale for ray-finned fish evolution.
    Proc Biol Sci. 2007 Feb 22;274(1609):489-98 PMID: 17476768
  22. [Micro vs. macro: structural-functional organization of avian micro- and macrochromosomes].
    Genetika. 1996 May;32(5):597-608 PMID: 8755033
  23. The C. savignyi genetic map and its integration with the reference sequence facilitates insights into chordate genome evolution.
    Genome Res. 2008 Aug;18(8):1369-79 PMID: 18519652
  24. Mutation rates in mammalian genomes.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):803-8 PMID: 11792858
  25. Highly conserved non-coding sequences are associated with vertebrate development.
    PLoS Biol. 2005 Jan;3(1):e7 PMID: 15630479
  26. A fine-scale map of recombination rates and hotspots across the human genome.
    Science. 2005 Oct 14;310(5746):321-4 PMID: 16224025
  27. How and why chromosome inversions evolve.
    PLoS Biol. 2010 Sep 28;8(9): PMID: 20927412
  28. The genetic architecture of parallel armor plate reduction in threespine sticklebacks.
    PLoS Biol. 2004 May;2(5):E109 PMID: 15069472
  29. An economic method for the fluorescent labeling of PCR fragments.
    Nat Biotechnol. 2000 Feb;18(2):233-4 PMID: 10657137
  30. In vivo enhancer analysis of human conserved non-coding sequences.
    Nature. 2006 Nov 23;444(7118):499-502 PMID: 17086198
  31. The Hill-Robertson effect: evolutionary consequences of weak selection and linkage in finite populations.
    Heredity (Edinb). 2008 Jan;100(1):19-31 PMID: 17878920
  32. Estimation of synteny conservation and genome compaction between pufferfish (Fugu) and human.
    Yeast. 2000 Apr;17(1):22-36 PMID: 10797599
  33. The sex-determining locus in the tiger pufferfish, Takifugu rubripes.
    Genetics. 2007 Apr;175(4):2039-42 PMID: 17287528
  34. Reciprocal gene loss between Tetraodon and zebrafish after whole genome duplication in their ancestor.
    Trends Genet. 2007 Mar;23(3):108-12 PMID: 17275132
  35. Paleontological evidence to date the tree of life.
    Mol Biol Evol. 2007 Jan;24(1):26-53 PMID: 17047029
  36. Near-neutrality in evolution of genes and gene regulation.
    Proc Natl Acad Sci U S A. 2002 Dec 10;99(25):16134-7 PMID: 12461171
  37. Characterization of Japanese flounder karyotype by chromosome bandings and fluorescence in situ hybridization with DNA markers.
    Genetica. 2007 Nov;131(3):267-74 PMID: 17273899
  38. Exceptionally high levels of recombination across the honey bee genome.
    Genome Res. 2006 Nov;16(11):1339-44 PMID: 17065604
  39. Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution.
    Nature. 2004 Dec 9;432(7018):695-716 PMID: 15592404
  40. Rearrangement rate following the whole-genome duplication in teleosts.
    Mol Biol Evol. 2007 Mar;24(3):860-7 PMID: 17218642
  41. Sex-specific recombination rates in zebrafish (Danio rerio).
    Genetics. 2002 Feb;160(2):649-57 PMID: 11861568
  42. Large-scale appearance of ultraconserved elements in tetrapod genomes and slowdown of the molecular clock.
    Mol Biol Evol. 2008 Feb;25(2):402-8 PMID: 18056681
  43. Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome.
    Nature. 1993 Nov 18;366(6452):265-8 PMID: 8232585
  44. A medaka gene map: the trace of ancestral vertebrate proto-chromosomes revealed by comparative gene mapping.
    Genome Res. 2004 May;14(5):820-8 PMID: 15078856
  45. A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates.
    Genetics. 2000 Jul;155(3):1331-45 PMID: 10880492
  46. The complete sequence of a heterochromatic island from a higher eukaryote. The Cold Spring Harbor Laboratory, Washington University Genome Sequencing Center, and PE Biosystems Arabidopsis Sequencing Consortium.
    Cell. 2000 Feb 4;100(3):377-86 PMID: 10676819
  47. Genome evolution and biodiversity in teleost fish.
    Heredity (Edinb). 2005 Mar;94(3):280-94 PMID: 15674378
  48. A genetic linkage map for the tiger pufferfish, Takifugu rubripes.
    Genetics. 2005 Sep;171(1):227-38 PMID: 15972462
  49. Genome of the marsupial Monodelphis domestica reveals innovation in non-coding sequences.
    Nature. 2007 May 10;447(7141):167-77 PMID: 17495919
  50. From 2R to 3R: evidence for a fish-specific genome duplication (FSGD).
    Bioessays. 2005 Sep;27(9):937-45 PMID: 16108068
  51. A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate.
    Genome Res. 2009 Mar;19(3):510-9 PMID: 19088305
  52. Extreme genomic variation in a natural population.
    Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5698-703 PMID: 17372217
  53. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype.
    Nature. 2004 Oct 21;431(7011):946-57 PMID: 15496914
  54. Highly conserved regulatory elements around the SHH gene may contribute to the maintenance of conserved synteny across human chromosome 7q36.3.
    Genomics. 2005 Aug;86(2):172-81 PMID: 15939571
  55. Fitness of hatchery-reared salmonids in the wild.
    Evol Appl. 2008 May;1(2):342-55 PMID: 25567636
  56. Genome-wide scans for footprints of natural selection.
    Philos Trans R Soc Lond B Biol Sci. 2010 Jan 12;365(1537):185-205 PMID: 20008396
  57. A high-resolution single nucleotide polymorphism genetic map of the mouse genome.
    PLoS Biol. 2006 Nov;4(12):e395 PMID: 17105354
  58. Adaptive evolution and explosive speciation: the cichlid fish model.
    Nat Rev Genet. 2004 Apr;5(4):288-98 PMID: 15131652
  59. Recombination difference between sexes: a role for haploid selection.
    PLoS Biol. 2005 Mar;3(3):e63 PMID: 15736976
  60. Imprinted chromosomal regions of the human genome have unusually high recombination rates.
    Genetics. 2003 Nov;165(3):1629-32 PMID: 14733198
  61. Reinterpreting pericentromeric heterochromatin.
    Curr Opin Plant Biol. 2006 Dec;9(6):647-53 PMID: 17015032
  62. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations.
    Genomics. 1987 Oct;1(2):174-81 PMID: 3692487
  63. GRIMM: genome rearrangements web server.
    Bioinformatics. 2002 Mar;18(3):492-3 PMID: 11934753
  64. Major events in the genome evolution of vertebrates: paranome age and size differ considerably between ray-finned fishes and land vertebrates.
    Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1638-43 PMID: 14757817
  65. A physical map of the papaya genome with integrated genetic map and genome sequence.
    BMC Genomics. 2009 Aug 07;10:371 PMID: 19664231
  66. Variation in sequence and organization of splicing regulatory elements in vertebrate genes.
    Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15700-5 PMID: 15505203
Article Info
Journal
Genome biology and evolution
Abbr.
Genome Biol Evol
ISSN
1759-6653
DOI
10.1093/gbe/evr041
Published
2011-00-00
Epub
2011-00-01
Pages
424-42
Language
English
Region
England
NLM ID
101509707
PMCID
PMC5654407
Subset
IM
External Links
PubMed source DOI: 10.1093/gbe/evr041 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2